Epigenetic Dynamics of Plant Aging: Nuclear Envelope Dysfunction and the Spatiotemporal Modulation of DNA Methylation in Arabidopsis

Aging is a multifactorial biological process characterized by a progressive decline in physiological function, accompanied by widespread molecular and epigenomic alterations. While disruption of nuclear envelope components causes premature aging syndromes such as progeria in humans, the evolutionary conservation and broader implications of nuclear architectural dysfunction during whole-plant aging remain largely unresolved. In particular, epigenetic drift—genome-wide alterations in chromatin organization, DNA methylation, and heterochromatin integrity—is a conserved hallmark of aging and progeroid conditions, yet its chromatin-state specificity, spatial distribution, and reversibility are poorly characterized in plants. In this thesis, I use Arabidopsis thaliana to dissect the molecular architecture of epigenomic aging, focusing on how nuclear envelope dysfunction—particularly loss of KAKU4 and CRWNs—accelerates age-associated phenotypes and drives genome-wide epigenetic instability. Through lifespan phenotyping and multi-omics profiling, I show that nuclear envelope defects promote transcriptional drift and impair heterochromatin maintenance, abolishing the normal age-linked accumulation of CHH methylation at transposable elements and across pericentromeric heterochromatin. To resolve methylation dynamics within individual plants, I establish a spatially resolved aerial rosette system induced by photoperiod reactivation and extend this analysis to the perennial-like soc1 ful mutant. I demonstrate that age-related CHH methylation at transposable elements is dependent on organ age and leaf developmental order, accumulating in basal rosettes but remaining attenuated in newly formed distal rosettes. Parallel analysis of dedifferentiated callus reveals sustained CHH hypomethylation and a failure to acquire age-linked methylation over time, recapitulating the epigenomic resilience of meristematic progenitors even under prolonged in vitro culture. Finally, by integrating tissue- and genotype-specific methylation trajectories, I define cytosine-level changes that consistently vary with age and remain comparatively stable in regenerative contexts. Although preliminary, these loci provide candidate markers for assessing epigenetic age in Arabidopsis and suggest that nuclear integrity and developmental state shape the balance between methylation drift and maintenance.